Sidestepping genealogical discordance: allele sharing as a basis for species delimitation

Jean-François Flot

Species delimitation aims to delineate the “elementary particles” of biodiversity,
i.e., species, and as such is a necessary prerequisite to studies in domains as diverse
as physiology, ecology or population genetics. However, although there is now a general
consensus that DNA-based approaches to species delimitation are often more reliable
than morphology-based ones (as DNA, unlike morphology, does not display plasticity
under the influence of the environment), there remains a profound disagreement about
how to delineate species, and even how best to define them.

Three main types of approaches to species delimitation have been proposed. Distance-based
approaches, such as DNA barcoding and ABGD (automatic barcode gap delimitation), rely
on the postulate that genetic distances within species are smaller than interspecific
distances; such approaches are the most frequently used to delineate microbial species,
be it from complete genome sequences or by sequencing one or several representative
genome regions (called “markers”). Tree-based approaches, such as generalized mixed
Yule-coalescent (GMYC) models or Poisson tree processes (PTP), attempt to distinguish
intraspecific vs. interspecific regions of phylogenetic trees under the assumption
that branching rates are markedly higher within species-level clades than between
them. Tree-based approaches are presently the most popular ones among botanists and
zoologists because they are best suited to analyze the large datasets amassed since
2003 for fast-evolving regions of the mitochondrial (for animals) or chloroplastic
(for plants) genomes thanks to the availability of near-universal PCR primers targeting
these regions. Finally, a third type of approach to species delimitation uses allele
sharing as a proxy for gene flow between individuals, and consider groups of individuals
that share a common set of alleles (“gene pool”) as conspecific. These allele sharing-based
approaches are closely related to the classical biological species criterion of interfecundity
and were therefore initially thought to apply only to sexually recombining species;
however, there is growing evidence that allele sharing is also informative on species
boundaries for organisms that do not perform meiotic sex but exchange genes horizontally,
such as bacteria and bdelloid rotifers. One additional advantage of allele sharing-based
approaches to species delimitation is that they do not assume concordant genealogies
among conspecific individuals: notably, they are not hindered by the species-level
non-monophyly in gene trees that often result from incomplete lineage sorting or introgressive
hybridization, and do not assume either that intraspecific distances are smaller than
interspecific distances. Last, but not least, allele sharing-based approaches are
very fast computationally (as they do not require all pairwise comparisons among sequences
in a dataset to be computed and do not involve phylogenetic tree reconstruction).
Hence, allele sharing has the potential to yield a one-size-fit-all, universal approach
to species delimitation, bringing together the presently very disparate taxonomic
practices of microbiologists, botanists and zoologists.